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      Prevalence and Epidemiology of Non-O157 Escherichia coli Serogroups O26, O103, O111, and O145 and Shiga Toxin Gene Carriage in Scottish Cattle, 2014–2015

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          Abstract

          Cattle are reservoirs for Shiga toxin Escherichia coli (STEC), bacteria shed in animal feces. Humans are infected through consumption of contaminated food or water and by direct contact, causing serious disease and kidney failure in the most vulnerable.

          ABSTRACT

          Cattle are a reservoir for Shiga toxin-producing Escherichia coli (STEC), zoonotic pathogens that cause serious clinical disease. Scotland has a higher incidence of STEC infection in the human population than the European average. The aim of this study was to investigate the prevalence and epidemiology of non-O157 serogroups O26, O103, O111, and O145 and Shiga toxin gene carriage in Scottish cattle. Fecal samples ( n = 2783) were collected from 110 herds in 2014 and 2015 and screened by real-time PCR. Herd-level prevalence (95% confidence interval [CI]) for O103, O26, and O145 was estimated as 0.71 (0.62, 0.79), 0.43 (0.34, 0.52), and 0.23 (0.16, 0.32), respectively. Only two herds were positive for O111. Shiga toxin prevalence was high in both herds and pats, particularly for stx 2 (herd level: 0.99; 95% CI: 0.94, 1.0). O26 bacterial strains were isolated from 36 herds on culture. Fifteen herds yielded O26 stx-positive isolates that additionally harbored the intimin gene; six of these herds shed highly pathogenic stx 2-positive strains. Multiple serogroups were detected in herds and pats, with only 25 herds negative for all serogroups. Despite overlap in detection, regional and seasonal effects were observed. Higher herd prevalence for O26, O103, and stx 1 occurred in the South West, and this region was significant for stx 2 at the pat level ( P = 0.015). Significant seasonal variation was observed for O145 prevalence, with the highest prevalence in autumn ( P = 0.032). Negative herds were associated with Central Scotland and winter. Herds positive for all serogroups were associated with autumn and larger herd size and were not housed at sampling.

          IMPORTANCE Cattle are reservoirs for Shiga toxin-producing Escherichia coli (STEC), bacteria shed in animal feces. Humans are infected through consumption of contaminated food or water and by direct contact, resulting in serious disease and kidney failure in the most vulnerable. The contribution of non-O157 serogroups to STEC illness was underestimated for many years due to the lack of specific tests. Recently, non-O157 human cases have increased, with O26 STEC of particular note. It is therefore vital to investigate the level and composition of non-O157 in the cattle reservoir and to compare them historically and by the clinical situation. In this study, we found cattle prevalence high for toxin, as well as for O103 and O26 serogroups. Pathogenic O26 STEC were isolated from 14% of study herds, with toxin subtypes similar to those seen in Scottish clinical cases. This study highlights the current risk to public health from non-O157 STEC in Scottish cattle.

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            The 4,639,221-base pair sequence of Escherichia coli K-12 is presented. Of 4288 protein-coding genes annotated, 38 percent have no attributed function. Comparison with five other sequenced microbes reveals ubiquitous as well as narrowly distributed gene families; many families of similar genes within E. coli are also evident. The largest family of paralogous proteins contains 80 ABC transporters. The genome as a whole is strikingly organized with respect to the local direction of replication; guanines, oligonucleotides possibly related to replication and recombination, and most genes are so oriented. The genome also contains insertion sequence (IS) elements, phage remnants, and many other patches of unusual composition indicating genome plasticity through horizontal transfer.
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              The European Union summary report on trends and sources of zoonoses, zoonotic agents and food‐borne outbreaks in 2016

              (2017)
              Abstract This report of the European Food Safety Authority and the European Centre for Disease Prevention and Control presents the results of the zoonoses monitoring activities carried out in 2016 in 37 European countries (28 Member States (MS) and nine non‐MS). Campylobacteriosis was the most commonly reported zoonosis and the increasing European Union (EU) trend for confirmed human cases since 2008 stabilised during 2012–2016. In food, the occurrence of Campylobacter remained high in broiler meat. The decreasing EU trend for confirmed human salmonellosis cases since 2008 ended during 2012–2016, and the proportion of human Salmonella Enteritidis cases increased. Most MS met their Salmonella reduction targets for poultry, except five MS for laying hens. At primary production level, the EU‐level flock prevalence of target Salmonella serovars in breeding hens, broilers, breeding and fattening turkeys decreased or stabilised compared with previous years but the EU prevalence of S. Enteritidis in laying hens significantly increased. In foodstuffs, the EU‐level Salmonella non‐compliance for minced meat and meat preparations from poultry was low. The number of human listeriosis confirmed cases further increased in 2016, despite the fact that Listeria seldom exceeds the EU food safety limit in ready‐to‐eat foods. The decreasing EU trend for confirmed yersiniosis cases since 2008 stabilised during 2012–2016, and also the number of confirmed Shiga toxin‐producing Escherichia coli (STEC) infections in humans was stable. In total, 4,786 food‐borne outbreaks, including waterborne outbreaks, were reported. Salmonella was the most commonly detected causative agent – with one out of six outbreaks due to S. Enteritidis – followed by other bacteria, bacterial toxins and viruses. Salmonella in eggs continued to represent the highest risk agent/food combination. The report further summarises trends and sources for bovine tuberculosis, brucellosis, trichinellosis, echinococcosis, toxoplasmosis, rabies, Q fever, West Nile fever and tularaemia.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                Appl Environ Microbiol
                Appl Environ Microbiol
                aem
                aem
                AEM
                Applied and Environmental Microbiology
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                0099-2240
                1098-5336
                12 March 2021
                27 April 2021
                May 2021
                27 April 2021
                : 87
                : 10
                : e03142-20
                Affiliations
                [a ]The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush, UK
                [b ]Moredun Research Institute, Edinburgh, UK
                [c ]Scottish E. coli, O157/STEC Reference Laboratory, Department of Laboratory Medicine, Royal Infirmary of Edinburgh, Edinburgh, UK
                [d ]The Pirbright Research Institute, Pirbright, Woking, UK
                [e ]Laboratoire de Biométrie et Biologie Evolutive, Université de Lyon, Villeurbanne, France
                [f ]Epidemiology Research Unit, Scotland’s Rural College (SRUC), An Lòchran, Inverness Campus, Inverness, UK
                INRS—Institut Armand-Frappier
                Author notes
                Address correspondence to Deborah V. Hoyle, deborah.hoyle@ 123456ed.ac.uk ; or Margo E. Chase-Topping, margo.chase@ 123456ed.ac.uk .

                Citation Hoyle DV, Keith M, Williamson H, Macleod K, Mathie H, Handel I, Currie C, Holmes A, Allison L, McLean R, Callaby R, Porphyre T, Tongue SC, Henry MK, Evans J, Gunn GJ, Gally DL, Silva N, Chase-Topping ME. 2021. Prevalence and epidemiology of non-O157 Escherichia coli serogroups O26, O103, O111, and O145 and Shiga toxin gene carriage in Scottish cattle, 2014–2015. Appl Environ Microbiol 87:e03142-20. https://doi.org/10.1128/AEM.03142-20.

                Author information
                https://orcid.org/0000-0002-2874-1551
                Article
                03142-20
                10.1128/AEM.03142-20
                8117755
                33712425
                020cc2a3-550c-4fda-9edb-0105d6fbb8ed
                Copyright © 2021 Hoyle et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                History
                : 4 January 2021
                : 1 March 2021
                Page count
                Figures: 6, Tables: 3, Equations: 0, References: 83, Pages: 18, Words: 12141
                Funding
                Funded by: Wellcome Trust, https://doi.org/10.13039/100004440;
                Award ID: 105832/Z/14/Z
                Award Recipient :
                Funded by: UKRI | Biotechnology and Biological Sciences Research Council (BBSRC), https://doi.org/10.13039/501100000268;
                Award ID: BBS/E/D/20002173
                Award Recipient : Award Recipient :
                Categories
                Public and Environmental Health Microbiology
                Custom metadata
                May 2021

                Microbiology & Virology
                shiga toxin-producing escherichia coli,non-o157,cattle,epidemiology
                Microbiology & Virology
                shiga toxin-producing escherichia coli, non-o157, cattle, epidemiology

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